Insect Biochemistry and Molecular Biology 30 2000 405–413 www.elsevier.comlocateibmb
Characterization of lipophorin binding to the midgut of larval Manduca sexta
Katia C. Gondim
1,2
, Michael A. Wells
Department of Biochemistry and Center for Insect Science, Biological Sciences West, University of Arizona, Tucson, AZ 85721, USA Received 17 May 1999; received in revised form 5 January 2000; accepted 10 January 2000
Abstract
Lipophorin binding to the midgut of Manduca sexta larvae was characterized in a midgut membrane preparation, using iodinated larval high-density lipophorin
125
I-HDLp-L. The iodination procedure did not change the affinity of the preparation for lipophorin. In the presence of increasing concentrations of membrane protein, corresponding increases in lipophorin binding were observed.
The time-course of lipophorin binding to the membranes was affected by the lipophorin concentration in the medium, and at a low lipoprotein concentration, a longer time was required for equilibrium to be reached. The specific binding of lipophorin to the midgut
membrane was a saturable process with a K
d
= 1.5
± 0.2
× 10
27
M and a maximal binding capacity =
127 ±
17 ng lipophorin µ
g of mem- brane protein. Binding did not depend on calcium, was maximal around pH 5.5, was strongly inhibited by an increase in the ionic
strength, and abolished by suramin. However, suramin did not completely displace lipophorin that was previously bound to the membrane preparation. The lipid content of the lipophorin did not significantly affect the affinity of the membrane preparation for
lipoprotein.
2000 Elsevier Science Ltd. All rights reserved.
Keywords: Lipophorin; Manduca sexta; Midgut; Lipoprotein
1. Introduction
Several classes of lipids—diacylglycerol, phospholip- ids, cholesterol, and hydrocarbons—are transported in
insect hemolymph by lipophorin, the major hemolymph lipoprotein Chino et al., 1981; Chino, 1985; Shapiro et
al., 1988; Soulages and Wells, 1994; Blacklock and Ryan, 1994. All lipophorins contain two apolipoprote-
ins, apolipophorin-I and -II apoLp-I and apoLp-II, and the adults of some species contain a third apolipoprotein,
apoLp-III Kanost et al., 1990; Van der Horst, 1990; Soulages and Wells, 1994. Lipophorin particles can
contain different amounts of lipids and are classified
Corresponding author. Tel.: +
1-520-621-3847; fax: +
1-520-621- 9288.
E-mail address: mawellsu.arizona.edu M.A. Wells.
1
Recipient of fellowships from Pew Charitable Trusts Latin Amer- ican Fellows Program and from Conselho Nacional de Desenvolvi-
mento Cientı´fico e Tecnologico CNPq, Brasil.
2
Permanent address: Departamento de Bioquı´mica Me´dica, Insti- tuto de Cieˆncias Biome´dicas, Universidade Federal do Rio de Janeiro,
RJ, Brasil.
0965-174800 - see front matter
2000 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 5 - 1 7 4 8 0 0 0 0 0 1 4 - X
according to their densities as HDLp high density lipophorin, LDLp low density lipophorin or VHDLp
very high density lipophorin Beenakkers et al., 1988. In some species, such as Manduca sexta and Locusta
migratoria, the lipophorin density depends on the life stage, as well as, the physiological situation of the insect
Prasad et al., 1986; Surholt et al., 1992.
During lipid delivery to different tissues, lipophorin apolipoproteins are not accumulated or degraded in the
organs, and can be reloaded with more lipids and reutil- ized, thus lipophorin acts as a reusable lipid shuttle
Downer and Chino, 1985; Van Heusden et al., 1987. It has been shown that lipophorin interaction with tissues
is mediated by specific binding sites Van Antwerpen et al., 1989; Atella et al. 1992, 1995, and in some experi-
ments it seems that lipid transfer occurs at the surface of the cells, without the particle internalization Van
Antwerpen et al., 1988; Machado et al., 1996. These data have lead to the suggestion that lipophorin binds to
the cell surface via a docking receptor, but not much is known about these putative receptors. A lipophorin
receptor from the fat body of M. sexta larvae was iso- lated and characterized Tsuchida and Wells, 1990, and
406 K.C. Gondim, M.A. Wells Insect Biochemistry and Molecular Biology 30 2000 405–413
the fat body receptor from L. migratoria was also studied Dantuma et al., 1996. On the other hand it has been
shown that lipophorin can be internalized into midgut Bauerfeind and Komnick, 1992 and fat body Dantuma
et al., 1997, 1999. Such observations might suggest the existence of a modified endocytotic cycle Dantuma et
al., 1998
In feeding M. sexta larvae, lipophorin cycles between the digestive tract, where lipids are absorbed from the
diet and transferred to the circulating lipoprotein, and the fat body, where the lipids are taken up and stored
Tsuchida and Wells, 1988. However, no lipophorin receptor from the digestive system has been studied. In
this paper, the binding of lipophorin to the midgut of larval M. sexta was characterized in order to understand
more completely the lipid transport system in this insect.
2. Materials and methods